Mast cell chemotaxis chemoattractants and signaling pathways

Frontiers in Immunology

Volumn 3, Issue MAY, 2012, Pages

  Halova, Ivana ^a   Draberova, Lubica ^a   Draber, Petr ^a  

^a INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

Author keywords

Cell migration; Chemoattractant; Chemotaxis; Ige receptor; Mast cell; Plasma membrane; Signal transduction

Indexed keywords

EID: 84874128352     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00119     Document Type: Review

References (190)

1. Abonia, J. P., Austen, K. F., Rollins, B. J., Joshi, S. K., Flavell, R. A., Kuziel, W. A., Koni, P. A., and Gurish, M. F. (2005). Constitutive homing of mast cell progenitors to the intestine depends on autologous expression of the chemokine receptor CXCR2. Blood 105, 4308-4313.
2. Amin, K., Janson, C., Harvima, I., Venge, P., and Nilsson, G. (2005). CC chemokine receptors CCR1 and CCR4 are expressed on airway mast cells in allergic asthma. J. Allergy Clin. Immunol. 116, 1383-1386.
3. Ancellin, N., Colmont, C., Su, J., Li, Q., Mittereder, N., Chae, S. S., Stefansson, S., Liau, G., and Hla, T. (2002). Extracellular export of sphingosine kinase-1 enzyme. Sphingosine 1-phosphate generation and the induction of angiogenic vascular maturation. J. Biol. Chem. 277, 6667-6675.
4. Andrew, N., and Insall, R. H. (2007). Chemotaxis in shallow gradients is mediated independently of PtdIns 3-kinase by biased choices between random protrusions. Nat. Cell Biol. 9, 193-200.
5. Angeli, V., Staumont, D., Charbonnier, A. S., Hammad, H., Gosset, P., Pichavant, M., Lambrecht, B. N., Capron, M., Dombrowicz, D., and Trottein, F. (2004). Activation of the D prostanoid receptor 1 regulates immune and skin allergic responses. J. Immunol. 172, 3822-3829.
6. Aung, G., Niyonsaba, F., Ushio, H., Kajiwara, N., Saito, H., Ikeda, S., Ogawa, H., and Okumura, K. (2011). Catestatin, a neuroendocrine antimicrobial peptide, induces human mast cell migration, degranulation and production of cytokines and chemokines. Immunology 132, 527-539.
7. Bautz, F., Denzlinger, C., Kanz, L., and Mohle, R. (2001). Chemotaxis and transendothelial migration of CD34+ hematopoietic progenitor cells induced by the inflammatory mediator leukotriene D4 are mediated by the 7-transmembrane receptor CysLT1. Blood 97, 3433-3440.
8. Berenbaum, F., Humbert, L., Bereziat, G., and Thirion, S. (2003). Concomitant recruitment of ERK1/2 and p38 MAPK signalling pathway is required for activation of cytoplasmic phospholipase A2 via ATP in articular chondrocytes. J. Biol. Chem. 278, 13680-13687.
9. Boehme, S. A., Franz-Bacon, K., Chen, E. P., Ly, T. W., Kawakami, Y., and Bacon, K. B. (2009). Murine bone marrow-derived mast cells express chemoattractant receptor-homologous molecule expressed on T-helper class 2 cells (CRTh2). Int. Immunol. 21, 621-632.
10. Boyce, J. A. (2007). Mast cells and eicosanoid mediators: a system of reciprocal paracrine and autocrine regulation. Immunol. Rev. 217, 168-185.
11. Brdička, T., Imrich, M., Angelisová, P., Brdičková, N., Horváth, O., Špička, J., Hilgert, I., Lusková, P., Dráber, P., Novák, P., Engels, N., Wienands, J., Simeoni, L., Osterreicher, J., Aguado, E., Malissen, M., Schraven, B., and Hořejší, V. (2002). Non-T cell activation linker (NTAL): a transmembrane adaptor protein involved in immunoreceptor signaling. J. Exp. Med. 196, 1617-1626.
12. Brightling, C. E., Ammit, A. J., Kaur, D., Black, J. L., Wardlaw, A. J., Hughes, J. M., and Bradding, P. (2005a). The CXCL10/CXCR3 axis mediates human lung mast cell migration to asthmatic airway smooth muscle. Am. J. Respir. Crit. Care Med. 171, 1103-1108.
13. Brightling, C. E., Kaur, D., Berger, P., Morgan, A. J., Wardlaw, A. J., and Bradding, P. (2005b). Differential expression of CCR3 and CXCR3 by human lung and bone marrowderived mast cells: implications for tissue mast cell migration. J. Leukoc. Biol. 77, 759-766.
14. Brown, R. A., Spina, D., and Page, C. P. (2008). Adenosine receptors and asthma. Br. J. Pharmacol. 153, S446S456.
15. Brzezińska-Blaszczyk, E., Pietrzak, A., and Misiak-Tloczek, A. H. (2007). Tumor necrosis factor (TNF) is a potent rat mast cell chemoattractant. J. Interferon Cytokine Res. 27, 911-920.
16. Buday, L., Egan, S. E., Rodriguez, V. P., Cantrell, D. A., and Downward, J. (1994). A complex of Grb2 adaptor protein, Sos exchange factor, and a 36-kDa membrane-bound tyrosine phosphoprotein is implicated in Ras activation in T cells. J. Biol. Chem. 269, 9019-9023.
17. Byrne, S. N, Limón-Flores, A. Y., and Ullrich, S. E. (2008). Mast cell migration from the skin to the draining lymph nodes upon ultraviolet irradiation represents a key step in the induction of immune suppression. J. Immunol. 180, 4648-4655.
18. Chabot, B., Stephenson, D. A., Chapman, V. M., Besmer, P., and Bernstein,A. (1988). The proto-oncogene c-kit encoding a transmembrane tyrosine kinase receptor maps to the mouse W locus. Nature 335, 88-89
19. Charest, P. G., and Firtel, R. A. (2010). "TORCing" neutrophil chemotaxis. Dev. Cell 19, 795-796.
20. Charest, P. G., Shen, Z., Lakoduk, A., Sasaki, A. T., Briggs, S. P., and Firtel, R. A. (2010). A Ras signaling complex controls the RasC-TORC2 pathway and directed cell migration. Dev. Cell 18, 737-749.
21. Chen, L., Iijima, M., Tang, M., Landree, M. A., Huang, Y. E., Xiong, Y., Iglesias, P. A., and Devreotes, P. N. (2007). PLA2 and PI3K/PTEN pathways act in parallel to mediate chemotaxis. Dev. Cell 12, 603-614.
22. Cho, K. J., Seo, J. M., Lee, M. G., and Kim, J. H. (2010). BLT2 Is upregulated in allergen-stimulated mast cells and mediates the synthesis of Th2 cytokines. J. Immunol. 185, 6329-6337.
23. Clark, J. D., Lin, L. L., Kriz, R. W., Ramesha, C. S., Sultzman, L. A., Lin, A. Y., Milona, N., and Knopf, J. L. (1991). A novel arachidonic acid-selective cytosolic PLA2 contains a Ca2+-dependent translocation domain with homology to PKC and GAP. Cell 65, 1043-1051.
24. Collington, S. J., Hallgren, J., Pease, J. E., Jones, T. G., Rollins, B. J., Westwick, J., Austen, K. F., Williams, T. J., Gurish, M. F., and Weller, C. L. (2010a). The role of the CCL2/CCR2 axis in mouse mast cell migration in vitro and in vivo. J. Immunol. 184, 6114-6123.
25. Collington, S. J., Westwick, J., Williams, T. J., and Weller, C. L. (2010b). The function of CCR3 on mouse bone marrow-derived mast cellsinvitro.Immunology 129, 115-124.
26. Collington, S. J., Williams, T. J., and Weller, C. L. (2011). Mechanisms underlying the localisation of mast cells in tissues. Trends Immunol. 32, 478-485.
27. Cooper, P. H., and Stanworth, D. R. (1976). Isolation of rat peritoneal mast cells in high yield and purity. Methods Cell. Biol. 14, 365-378.
28. de Paulis, A., Annunziato, F., Di Gioia, L., Romagnani, S., Carfora, M., Beltrame, C., Marone, G., and Romagnani, P. (2001) Expression of the chemokine receptor CCR3 on human mast cells. Int. Arch. Allergy Immunol. 124, 146-150.
29. Dorsam, R. T., and Gutkind, J. S. (2007). G-protein-coupled receptors and cancer. Nat. Rev. Cancer 7, 79-94.
30. Dráber, P., and Dráberová, L. (2005). Lifting the fog in store-operated Ca2+ entry. Trends Immunol. 26, 621-624.
31. Draber, P., Halova, I., Levi-Schaffer, F., and Draberova, L. (2012). Transmembrane adaptor proteins in the high-affinity IgE receptor signaling. Front. Immun. 2:95. doi:10.3389/fimmu.2011.00095
32. + channel KCa3.1 in human lung mast cells and inhibits their migration via the adenosine A2A receptor. Eur. J. Immunol. 37, 1653-1662.
33. Eiseman, E., and Bolen, J. B. (1992). Engagement of the high-affinity IgE receptor activates src proteinrelated tyrosine kinases. Nature 355, 78-80.
34. Ferguson, G. J., Milne, L., Kulkarni, S., Sasaki, T., Walker, S., Andrews, S., Crabbe, T., Finan, P., Jones, G., Jackson, S., Camps, M., Rommel, C., Wymann, M., Hirsch, E., Hawkins, P., and Stephens, L. (2007). PI(3)Kγ has an important context-dependent role in neutrophil chemokinesis. Nat. Cell Biol. 9, 86-91.
35. Feuser, K., Thon, K.-P., Bischoff, S. C., and Lorentz, A. (2012). Human intestinal mast cells are a potent source of multiple chemokines. Cytokine 58, 178-185.
36. Finco, T. S., Kadlecek, T., Zhang, W., Samelson,L. E.,andWeiss,A. (1998). LAT is required for TCR-mediated activation of PLCγ1 and the Ras pathway. Immunity 9, 617-626.
37. Fox, C. C., Dvorak, A. M., Peters, S. P., Kagey-Sobotka, A., and Lichtenstein, L. M. (1985). Isolation and characterization of human intestinal mucosal mast cells. J. Immunol. 135, 483-491.
38. Funamoto, S., Meili, R., Lee, S., Parry, L., and Firtel, R. A. (2002). Spatial and temporal regulation of 3phosphoinositides by PI 3-kinase and PTEN mediates chemotaxis. Cell 109, 611-623.
39. Funamoto, S., Milan, K., Meili, R., and Firtel, R. A. (2001). Role of phosphatidylinositol 3' kinase and a downstream pleckstrin homology domain-containing protein in controlling chemotaxis in Dictyostelium. J. Cell Biol. 153, 795-810.
40. Furumoto, Y., Brooks, S., Olivera, A., Takagi, Y., Miyagishi, M., Taira, K., Casellas, R., Beaven, M. A., Gilfillan, A. M., and Rivera, J. (2006). Cutting edge: lentiviral short hairpin RNA silencing of PTEN in human mast cells reveals constitutive signals that promote cytokine secretion and cell survival. J. Immunol. 176, 5167-5171.
41. Ghebrehiwet, B., Kew, R. R., Gruber, B. L., Marchese, M. J., Peerschke, E. I., and Reid, K. B. (1995). Murine mast cells express two types of C1q receptors that are involved in the induction of chemotaxis and chemokinesis. J. Immunol. 155, 2614-2619.
42. Gilliland, L. K., Schieven, G. L., Norris, N. A., Kanner, S. B., Aruffo, A., and Ledbetter, J. A. (1992). Lymphocyte lineage-restricted tyrosinephosphorylated proteins that bind PLCγ1 SH2 domains. J. Biol. Chem. 267, 13610-13616.
43. Gomi, K., Zhu, F. G., and Marshall, J. S. (2000). Prostaglandin E2 selectively enhances the IgE-mediated production of IL-6 and granulocytemacrophage colony-stimulating factor by mast cells through an EP1/EP3-dependent mechanism. J. Immunol. 165, 6545-6552.
44. Gruber, B. L., Marchese, M. J., and Kew, R. R. (1994). Transforming growth factor-β1 mediates mast cell chemotaxis. J. Immunol. 152, 5860-5867.
45. Haddon, D. J., Antignano, F., Hughes, M. R., Blanchet, M. R., Zbytnuik, L., Krystal, G., and McNagny, K. M. (2009). SHIP1 is a repressor of mast cell hyperplasia, cytokine production, and allergic inflammation in vivo. J. Immunol. 183, 228-236.
46. Hájková, Z., Bugajev, V., Dráberová, E., Vinopal, S., Dráberová, L., Janáček, J., Dráber, P., and Dráber, P. (2011). STIM1-directed reorganization of microtubules in activated mast cells. J. Immunol. 186, 913-923.
47. Hallgren, J., and Gurish, M. F. (2007). Pathways of murine mast cell development and trafficking: tracking the roots and routes of the mast cell. Immunol. Rev. 217, 8-18.
48. Hallgren, J., and Gurish, M. F. (2011). Mast cell progenitor trafficking and maturation. Adv. Exp. Med. Biol. 716, 14-28.
49. Hallgren, J., Jones, T. G., Abonia, J. P., Xing, W., Humbles, A., Austen, K. F., and Gurish, M. F. (2007). Pulmonary CXCR2 regulates VCAM1 and antigen-induced recruitment of mast cell progenitors. Proc. Natl. Acad. Sci. U.S.A. 104, 20478-20483.
50. Hammad, H., de Heer, H. J., Soullie, T., Hoogsteden, H. C., Trottein, F., and Lambrecht, B. N. (2003). Prostaglandin D2 inhibits airway dendritic cell migration and function in steady state conditions by selective activation of the D prostanoid receptor 1. J. Immunol. 171, 3936-3940.
51. Hartmann, K., Henz, B. M., KrugerKrasagakes, S., Kohl, J., Burger, R., Guhl, S., Haase, I., Lippert, U., and Zuberbier, T. (1997). C3a and C5a stimulate chemotaxis of human mast cells. Blood 89, 2863-2870.
52. Heit, B., Liu, L., Colarusso, P., Puri, K. D., and Kubes, P. (2008). PI3K accelerates, but is not required for, neutrophil chemotaxis to fMLP. J. Cell Sci. 121, 205-214.
53. Heit, B., Tavener, S., Raharjo, E., and Kubes, P. (2002). An intracellular signaling hierarchy determines direction of migration in opposing chemotactic gradients. J. Cell Biol. 159, 91-102.
54. Hirai, H., Tanaka, K., Yoshie, O., Ogawa, K., Kenmotsu, K., Takamori, Y., Ichimasa, M., Sugamura, K., Nakamura, M., Takano, S., and Nagata, K. (2001). Prostaglandin D2 selectively induces chemotaxis in T helper type 2 cells, eosinophils, and basophils via seven-transmembrane receptor CRTH2. J. Exp. Med. 193, 255-261.
55. Huang, Y. E., Iijima, M., Parent, C. A., Funamoto, S., Firtel, R. A., and Devreotes, P. (2003). Receptormediated regulation of PI3Ks confines PI(3,4,5)P3 to the leading edge of chemotaxing cells. Mol. Biol. Cell 14, 1913-1922.
56. Humbles, A. A., Lu, B., Friend, D. S., Okinaga, S., Lora, J., Al-Garawi, A., Martin, T. R., Gerard, N. P., and Gerard, C. (2002). The murine CCR3 receptor regulates both the role of eosinophils and mast cells in allergen-induced airway inflammation and hyperresponsiveness. Proc. Natl. Acad. Sci. U.S.A 99, 1479-1484.
57. Ichikawa, A., Sugimoto, Y., and Negishi, M. (1996). Molecular aspects of the structures and functions of the prostaglandin E receptors. J. Lipid Mediat. Cell Signal. 14, 83-87.
58. Iijima, M., Huang, Y. E., and Devreotes, P. (2002). Temporal and spatial regulation of chemotaxis. Dev. Cell 3, 469-478.
59. Iijima, M., Huang, Y. E., Luo, H. R., Vazquez, F., and Devreotes, P. N. (2004). Novel mechanism of PTEN regulation by its phosphatidylinositol 4,5-bisphosphate binding motif is critical for chemotaxis. J. Biol. Chem. 279, 16606-16613.
60. Inamura, H., Kurosawa, M., Okano, A., Kayaba, H., and Majima, M. (2002). Expression of the interleukin-8 receptors CXCR1 and CXCR2 on cord-blood-derived cultured human mast cells. Int. Arch. Allergy Immunol. 128, 142-150.
61. Insall, R. H. (2010). Understanding eukaryotic chemotaxis: a pseudopod-centred view. Nat. Rev. Mol. Cell Biol. 11, 453-458.
62. Ishiai,M.,Kurosaki,M.,Inabe,K.,Chan, A. C., Sugamura, K., and Kurosaki, T. (2000). Involvement of LAT, Gads, and Grb2 in compartmentation of SLP-76 to the plasma membrane. J. Exp. Med. 192, 847-856.
63. Ishizuka, T., Okajima, F., Ishiwara, M., Iizuka, K., Ichimonji, I., Kawata, T., Tsukagoshi, H., Dobashi, K., Nakazawa, T., and Mori, M. (2001). Sensitized mast cells migrate toward the antigen: a response regulated by p38 mitogenactivated protein kinase and Rho-associated coiled-coil-forming protein kinase. J. Immunol. 167, 2298-2304.
64. Janssen, E., Zhu, M., Zhang, W., Koonpaew, S., and Zhang,W. (2003). LAB: a new membrane-associated adaptor molecule in B cell activation. Nat. Immunol. 4, 117-123.
65. Jensen, B. M., Beaven, M. A., Iwaki, S., Metcalfe, D. D., and Gilfillan, A. M. (2008). Concurrent inhibition of kitand FcεRI-mediated signaling: coordinated suppression of mast cell activation. J. Pharmacol. Exp. Ther. 324, 128-138.
66. Jiang, Y., Borrelli, L. A., Kanaoka, Y., Bacskai, B. J., and Boyce, J. A. (2007). CysLT2 receptors interact with CysLT1 receptors and downmodulate cysteinyl leukotriene dependent mitogenic responses of mast cells. Blood 110, 3263-3270.
67. Jiang, Y., Kanaoka, Y., Feng, C., Nocka, K., Rao, S., and Boyce, J. A. (2006). Cutting edge: Interleukin 4dependent mast cell proliferation requires autocrine/intracrine cysteinyl leukotriene-induced signaling. J. Immunol. 177, 2755-2759.
68. Jolly, P. S., Bektas, M., Olivera, A., Gonzalez-Espinosa, C., Proia, R. L., Rivera, J., Milstien, S., and Spiegel, S. (2004). Transactivation of sphingosine-1-phosphate receptors by FcεRI triggering is required for normal mast cell degranulation and chemotaxis. J. Exp. Med. 199, 959-970.
69. Jolly, P. S., Bektas, M., Watterson, K. R., Sankala, H., Payne, S. G., Milstien, S., and Spiegel, S. (2005). Expression of SphK1 impairs degranulation and motility of RBL-2H3 mast cells by desensitizing S1P receptors. Blood 105, 4736-4742.
70. Juremalm, M., Hjertson, M., Olsson, N., Harvima,I.,Nilsson,K.,and Nilsson, G. (2000). The chemokine receptor CXCR4 is expressed within the mast cell lineage and its ligand stromal cell-derived factor-1α acts as a mast cell chemotaxin. Eur. J. Immunol. 30, 3614-3622.
71. Juremalm, M., and Nilsson, G. (2005). Chemokine receptor expression by mast cells. Chem. Immunol. Allergy 87, 130-144.
72. Juremalm, M., Olsson, N., and Nilsson, G. (2002). Selective CCL5/RANTESinduced mast cell migration through interactions with chemokine receptors CCR1 and CCR4. Biochem. Biophys. Res. Commun. 297, 480-485.
73. Kanegasaki, S., Nomura, Y., Nitta, N., Akiyama, S., Tamatani, T., Goshoh, Y., Yoshida, T., Sato, T., and Kikuchi, Y. (2003). A novel optical assay system for the quantitative measurement of chemotaxis. J. Immunol. Methods 282, 1-11.
74. Kaplan, A. P. (2001). Chemokines, chemokine receptors and allergy. Int. Arch. Allergy Immunol. 124, 423-431.
75. Kay, L. J., Yeo, W. W., and Peachell, P. T. (2006). Prostaglandin E2 activates EP2 receptors to inhibit human lung mast cell degranulation. Br. J. Pharmacol. 147, 707-713.
76. Kay, R. R., Langridge, P., Traynor, D., and Hoeller, O. (2008). Changing directions in the study of chemotaxis. Nat. Rev. Mol. Cell Biol. 9, 455-463.
77. Kim,M. S.,Kuehn,H. S.,Metcalfe,D. D., and Gilfillan, A. M. (2008a). Activation and function of the mTORC1 pathway in mast cells. J. Immunol. 180, 4586-4595.
78. Kim, M. S., Rådinger, M., and Gilfillan, A. M. (2008b). The multiple roles of phosphoinositide 3-kinase in mast cell biology.Trends Immunol. 29, 493-501.
79. Kitaura, J., Eto, K., Kinoshita, T., Kawakami, Y., Leitges, M., Lowell, C. A., and Kawakami, T. (2005a). Regulation of highly cytokinergic IgEinduced mast cell adhesion by Src, Syk, Tec, and protein kinase C family kinases. J. Immunol. 174,4495-4504.
80. Kitaura, J., Kinoshita, T., Matsumoto, M., Chung, S., Kawakami, Y., Leitges, M., Wu, D., Lowell, C. A., and Kawakami, T. (2005b). IgEand IgE+Ag-mediated mast cell migration in an autocrine/paracrine fashion. Blood 105, 32223229.
81. Kolsch, V., Charest, P. G., and Firtel, R. A. (2008). The regulation of cell motility and chemotaxis by phospholipid signaling. J. Cell Sci. 121, 551-559.
82. Kortholt, A., Kataria, R., KeizerGunnink, I., van Egmond, W. N., Khanna, A., and van Haastert, P. J. (2011). Dictyostelium chemotaxis: essential Ras activation and accessory signalling pathways for amplification. EMBO Rep. 12, 1273-1279.
83. Kramer, R. M., and Sharp, J. D. (1995). Recent insights into the structure, function and biology of cPLA2. Agents Actions Suppl. 46, 65-76.
84. Kramer, R. M., and Sharp, J. D. (1997). Structure, function and regulation of Ca2+-sensitive cytosolic phospholipase A2 (cPLA2). FEBS Lett. 410, 49-53.
85. Kuehn,H. S.,and Gilfillan,A. M. (2007). G protein-coupled receptors and the modification of FcεRI-mediated mast cell activation. Immunol. Lett. 113, 59-69.
86. Kuehn, H. S., Jung, M. Y., Beaven, M. A., Metcalfe, D. D., and Gilfillan, A. M. (2011a). Distinct PGE2responder and non-responder phenotypes in human mast cell populations: all or nothing enhancement of antigen-dependent mediator release. Immunol. Lett. 141, 45-54.
87. Kuehn, H. S., Jung, M. Y., Beaven, M. A., Metcalfe, D. D., and Gilfillan, A. M. (2011b). Prostaglandin E2 activates and utilizes mTORC2 as a central signaling locus for the regulation of mast cell chemotaxis and mediator release. J. Biol. Chem. 286, 391-402.
88. Kuehn,H. S.,Rådinger,M.,Brown,J. M., Ali, K., Vanhaesebroeck, B., Beaven, M. A., Metcalfe, D. D., and Gilfillan, A. M. (2010). Btk-dependent Rac activation and actin rearrangement following FcεRI aggregation promotes enhanced chemotactic responses of mast cells. J. Cell Sci. 123, 2576-2585.
89. Kuehn, H. S., Swindle, E. J., Kim, M. S., Beaven, M. A., Metcalfe, D. D., and Gilfillan, A. M. (2008). The phosphoinositide 3-kinase-dependent activation of Btk is required for optimal eicosanoid production and generation of reactive oxygen species in antigen-stimulated mast cells. J. Immunol. 181, 7706-7712.
90. Kushnir-Sukhov, N. M., Gilfillan, A. M., Coleman, J. W., Brown, J. M., Bruening, S., Toth, M., and Metcalfe, D. D. (2006). 5-hydroxytryptamine induces mast cell adhesion and migration. J. Immunol. 177, 6422-6432.
91. Lee, S., Comer, F. I., Sasaki, A., McLeod, I. X., Duong, Y., Okumura, K., Yates, J. R. III, Parent, C. A., and Firtel, R. A. (2005). TOR complex 2integratescellmovementduring chemotaxis and signal relay in Dictyostelium. Mol. Biol. Cell 16, 4572-4583.
92. Lewis, R. A., Soter, N. A., Diamond, P. T., Austen, K. F., Oates, J. A., and Roberts, L. J. (1982). Prostaglandin D2 generation after activation of rat and human mast cells with anti-IgE. J. Immunol. 129, 1627-1631.
93. Linnekin, D., DeBerry, C. S., and Mou, S. (1997). Lyn associates with the juxtamembrane region of c-Kit and is activated by stem cell factor in hematopoietic cell lines and normal progenitor cells. J. Biol. Chem. 272, 27450-27455.
94. Liou, J., Kim, M. L., Heo, W. D., Jones, J. T., Myers, J. W., Ferrell, J. E. Jr., and Meyer, T. (2005). STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr. Biol. 15, 1235-1241.
95. Liu, H., Toman, R. E., Goparaju, S. K., Maceyka, M., Nava, V. E., Sankala, H., Payne, S. G., Bektas, M., Ishii, I., Chun, J., Milstien, S., and Spiegel, S. (2003). Sphingosine kinase type 2 is a putative BH3-only protein that induces apoptosis. J. Biol. Chem. 278, 40330-40336.
96. Liu, L., Das, S., Losert,W., and Parent, C. A. (2010). mTORC2 regulates neutrophil chemotaxis in a cAMPand RhoA-dependent fashion. Dev. Cell 19, 845-857.
97. Liu, L., and Parent, C. A. (2011). Review series: TOR kinase complexes and cell migration. J. Cell Biol. 194, 815-824.
98. Liu, S. K., Fang, N., Koretzky, G. A., and McGlade, C. J. (1999). The hematopoietic-specific adaptor protein gads functions in T-cell signaling via interactions with the SLP76 and LAT adaptors. Curr. Biol. 9, 67-75.
99. Lloyd, C. M., and Brown, Z. (2006). Chemokine receptors: therapeutic potential in asthma. Treat. Respir. Med. 5, 159-166.
100. Loovers, H. M., Postma, M., KeizerGunnink, I., Huang,Y. E., Devreotes, P. N., and van Haastert, P. J. (2006). Distinct roles of PI(3,4,5)P3 during chemoattractant signaling in Dictyostelium: a quantitative in vivo analysis by inhibition of PI3-kinase. Mol. Biol. Cell 17, 1503-1513.
101. Lundeen,K. A.,Sun,B.,Karlsson,L.,and Fourie,A. M. (2006). Leukotriene B4 receptors BLT1 and BLT2: expression and function in human and murine mast cells. J. Immunol. 177, 3439-3447.
102. Mathes, C., Fleig, A., and Penner, R. (1998). Calcium release-activated calcium current (ICRAC) is a direct target for sphingosine. J. Biol. Chem. 273, 25020-25030.
103. Matsui, K., and Nishikawa, A. (2005). Percutaneous application of peptidoglycan from Staphylococcus aureus induces an increase in mast cell numbers in the dermis of mice. Clin. Exp. Allergy 35, 382-387.
104. McCloskey, M. A., Fan, Y., and Luther, S. (1999). Chemotaxis of rat mast cells toward adenine nucleotides. J. Immunol. 163, 970-977.
105. Meininger, C. J., Yano, H., Rottapel, R., Bernstein, A., Zsebo, K. M., and Zetter, B. R. (1992). The c-kit receptor ligand functions as a mast cell chemoattractant. Blood 79,958-963.
106. Melendez, A. J., and Khaw, A. K. (2002). Dichotomy of Ca2+ signals triggered by different phospholipid pathways in antigen stimulation of human mast cells. J. Biol. Chem. 277, 17255-17262.
107. Mellor,E. A.,Frank,N.,Soler,D.,Hodge, M. R., Lora, J. M., Austen, K. F., and Boyce, J. A. (2003). Expression of the type 2 receptor for cysteinyl leukotrienes (CysLT2R) by human mast cells: functional distinction from CysLT1R. Proc. Natl. Acad. Sci. U.S.A. 100, 11589-11593.
108. Misiak-Tloczek, A., and BrzezińskaBlaszczyk, E. (2009). IL-6, but not IL-4, stimulates chemokinesis and TNF stimulates chemotaxis of tissue mast cells: involvement of both mitogen-activated protein kinases and phosphatidylinositol 3-kinase signalling pathways. APMIS 117, 558-567.
109. Mizugishi, K., Yamashita, T., Olivera, A., Miller, G. F., Spiegel, S., and Proia, R. L. (2005). Essential role for sphingosine kinases in neural and vascular development. Mol. Cell Biol. 25, 11113-11121.
110. Möhle, R., Bautz, F., Denzlinger, C., and Kanz, L. (2001). Transendothelial migration of hematopoietic progenitor cells. Role of chemotactic factors. Ann. N. Y. Acad. Sci. 938, 26-34.
111. Narumiya, S., and Watanabe, N. (2009). Migration without a clutch. Nat. Cell Biol. 11, 1394-1396.
112. Nataraj, C., Thomas, D. W., Tilley, S. L., Nguyen, M. T., Mannon, R., Koller, B. H., and Coffman, T. M. (2001). Receptors for prostaglandin E2 that regulate cellular immune responses in the mouse. J. Clin. Invest. 108, 1229-1235.
113. Nguyen, J. T., Porter, M., Amoui, M., Miller, W. T., Zuckermann, R. N., and Lim, W. A. (2000). Improving SH3 domain ligand selectivity using a non-natural scaffold. Chem. Biol. 7, 463-473.
114. Nilsson, G., Butterfield, J. H., Nilsson, K., and Siegbahn, A. (1994). Stem cell factor is a chemotactic factor for human mast cells. J. Immunol. 153, 3717-3723.
115. Nilsson, G., Hjertson, M., Andersson, M., Greiff, L., Svensson, C., Nilsson, K.,and Siegbahn,A. (1998). Demonstration of mast-cell chemotactic activity in nasal lavage fluid: characterization of one chemotaxin as c-kit ligand, stem cell factor. Allergy 53, 874-879.
116. Nilsson, G., Johnell, M., Hammer, C. H., Tiffany, H. L., Nilsson, K., Metcalfe, D. D., Siegbahn, A., and Murphy, P. M. (1996). C3a and C5a are chemotaxins for human mast cells and act through distinct receptors via a pertussis toxin-sensitive signal transduction pathway. J. Immunol. 157, 1693-1698.
117. Nilsson, G., Metcalfe, D. D., and Taub, D. D. (2000). Demonstration that platelet-activating factor is capable of activating mast cells and inducing a chemotactic response. Immunology 99, 314-319.
118. Nishio,M.,Watanabe,K.,Sasaki,J.,Taya, C., Takasuga, S., Iizuka, R., Balla, T., Yamazaki,M.,Watanabe,H.,Itoh,R., Kuroda, S., Horie,Y., Forster, I., Mak, T.W.,Yonekawa,H.,Penninger,J. M., Kanaho, Y., Suzuki, A., and Sasaki, T. (2007). Control of cell polarity and motility by the PtdIns(3,4,5)P3 phosphatase SHIP1. Nat. Cell Biol. 9, 36-44.
119. Ochi, H., Hirani, W. M., Yuan, Q., Friend, D. S., Austen, K. F., and Boyce, J. A. (1999). T helper cell type 2 cytokine-mediated comitogenic responses and CCR3 expression during differentiation of human mast cellsinvitro.J. Exp. Med. 190, 267-280.
120. Ohnishi, H., Miyahara, N., and Gelfand, E. W. (2008). The role of leukotriene B4 in allergic diseases. Allergol. Int. 57, 291-298.
121. Okayama, Y., and Kawakami, T. (2006). Development, migration, and survival of mast cells. Immunol. Res. 34, 97-115.
122. Oliveira, S. H., and Lukacs, N. W. (2001). Stem cell factor and IgEstimulated murine mast cells produce chemokines (CCL2, CCL17, CCL22) and express chemokine receptors. Inflamm. Res. 50, 168-174.
123. Olivera, A. (2008). Unraveling the complexities of sphingosine-1phosphate function: the mast cell model. Prostaglandins Other Lipid Mediat. 86, 1-11.
124. Olivera, A., Kohama, T., Edsall, L., Nava, V., Cuvillier, O., Poulton, S., and Spiegel, S. (1999). Sphingosine kinase expression increases intracellular sphingosine-1-phosphate and promotes cell growth and survival. J. Cell Biol. 147, 545-558.
125. Olivera, A., Mizugishi, K., Tikhonova, A., Ciaccia, L., Odom, S., Proia, R. L., and Rivera, J. (2007). The sphingosine kinase-sphingosine-1phosphate axis is a determinant of mast cell function and anaphylaxis. Immunity 26, 287-297.
126. Olivera, A., and Rivera, J. (2005). Sphingolipids and the balancing of immune cell function: lessons from the mast cell. J. Immunol. 174, 1153-1158.
127. Olivera, A., and Spiegel, S. (2001). Sphingosine kinase: a mediator of vital cellular functions. Prostaglandins 64, 123-134.
128. Olivera, A., Urtz, N., Mizugishi, K., Yamashita, Y., Gilfillan, A. M., Furumoto, Y., Gu, H., Proia, R. L., Baumruker, T., and Rivera, J. (2006). IgEdependent activation of sphingosine kinases 1 and 2 and secretion of sphingosine 1-phosphate requires Fyn kinase and contributes to mast cell responses. J. Biol. Chem. 281, 2515-2525.
129. Olsson, N., Rak, S., and Nilsson, G. (2000). Demonstration of mast cell chemotactic activity in bronchoalveolar lavage fluid collected from asthmatic patients before and during pollen season. J. Allergy Clin. Immunol. 105, 455-461.
130. Osher,E.,Weisinger,G.,Limor,R.,Tordjman, K., and Stern, N. (2006). The 5 lipoxygenase system in the vasculature: emerging role in health and disease. Mol. Cell Endocrinol. 252, 201-206.
131. Oskeritzian, C. A., Alvarez, S. E., Hait, N. C., Price, M. M., Milstien, S., and Spiegel, S. (2008). Distinct roles of sphingosine kinases 1 and 2 in human mast-cell functions. Blood 111, 4193-4200.
132. Papadopoulos, E. J., Fitzhugh, D. J., Tkaczyk, C., Gilfillan, A. M., Sassetti, C., Metcalfe, D. D., and Hwang, S. T. (2000). Mast cells migrate, but do not degranulate, in response to fractalkine, a membrane-bound chemokine expressed constitutively in diverse cells of the skin. Eur. J. Immunol. 30, 2355-2361.
133. Papakonstanti, E. A., Ridley, A. J., and Vanhaesebroeck, B. (2007). The p110δ isoform of PI 3-kinase negatively controls RhoA and PTEN. EMBO J. 26, 3050-3061.
134. Parravicini, V., Gadina, M., Kovarova, M., Odom, S., Gonzalez-Espinosa, C., Furumoto, Y., Saitoh, S., Samelson, L. E., O'Shea, J. J., and Rivera, J. (2002). Fyn kinase initiates complementary signals required for IgE-dependent mast cell degranulation. Nat. Immunol. 3, 741-748.
135. Peest, U., Sensken, S. C., Andreani, P., Hanel, P., Van Veldhoven, P. P., and Graler, M. H. (2008). S1P-lyase independent clearance of extracellular sphingosine 1-phosphate after dephosphorylation and cellular uptake. J. Cell Biochem. 104, 756-772.
136. Pietrzak, A., Wierzbicki, M., Wiktorska, M., and Brzezinska-Blaszczyk, E. (2011). Surface TLR2 and TLR4 expression on mature rat mast cells can be affected by some bacterial components and proinflammatory cytokines. Mediators Inflamm. 2011, 427473.
137. Poole, T. J., and Zetter, B. R. (1983). Stimulation of rat peritoneal mast cell migration by tumor-derived peptides. Cancer Res. 43, 58575861.
138. Ralevic, V., and Burnstock, G. (1998). Receptors for purines and pyrimidines. Pharmacol. Rev. 50, 413-492.
139. Ramkumar, V., Stiles, G. L., Beaven, M. A.,and Ali,H. (1993). The A3 adenosine receptor is the unique adenosine receptor which facilitates release of allergic mediators in mast cells. J. Biol. Chem. 268, 16887-16890.
140. Razin, E., Cordon-Cardo, C., and Good, R. A. (1981). Growth of a pure population of mouse mast cells in vitro with conditioned medium derived from concanavalin A-stimulated splenocytes. Proc. Natl. Acad. Sci. U.S.A. 78, 2559-2561.
141. Razin, E., Mencia-Huerta, J. M., Stevens, R. L., Lewis, R. A., Liu, F. T., Corey, E., and Austen, K. F. (1983). IgEmediated release of leukotriene C4, chondroitin sulfate E proteoglycan, β-hexosaminidase, and histamine from cultured bone marrow-derived mouse mast cells. J. Exp. Med. 157, 189-201.
142. Renkawitz, J., Schumann, K., Weber, M., Lämmermann, T., Pflicke, H., Piel, M., Polleux, J., Spatz, J. P., and Sixt, M. (2009). Adaptive force transmission in amoeboid cell migration. Nat. Cell Biol. 11, 1438-1443.
143. Rivera, J., Proia, R. L., and Olivera, A. (2008). The alliance of sphingosine1-phosphate and its receptors in immunity. Nat. Rev. Immunol. 8, 753-763.
144. Romagnani, P., de Paulis, A., Beltrame, C., Annunziato, F., Dente, V., Maggi, E., Romagnani, S., and Marone, G. (1999). Tryptase-chymase doublepositive human mast cells express the eotaxin receptor CCR3 and are attracted by CCR3-binding chemokines. Am. J. Pathol. 155, 1195-1204.
145. Romagnani, S. (2002). Cytokines and chemoattractants in allergic inflammation. Mol. Immunol. 38, 881-885.
146. Roos, J., DiGregorio, P. J., Yeromin, A. V., Ohlsen, K., Lioudyno, M., Zhang, S., Safrina, O., Kozak, J. A., Wagner, S. L., Cahalan, M. D., Velicelebi, G., and Stauderman, K. A. (2005). STIM1, an essential and conserved component of store-operated Ca2+ channel function. J. Cell Biol. 169, 435-445.
147. Roskoski, R. Jr. (2005). Signaling by Kit protein-tyrosine kinase-the stem cell factor receptor. Biochem. Biophys. Res. Commun. 337, 1-13.
148. Ruschpler, P., Lorenz, P., Eichler, W., Koczan, D., Hanel, C., Scholz, R., Melzer, C., Thiesen, H. J., and Stiehl, P. (2003). High CXCR3 expression in synovial mast cells associated with CXCL9 and CXCL10 expression in inflammatory synovial tissues of patients with rheumatoid arthritis. Arthritis Res. Ther. 5,R241R252.
149. Sabroe, I., Lloyd, C. M., Whyte, M. K., Dower, S. K., Williams, T. J., and Pease, J. E. (2002). Chemokines, innate and adaptive immunity, and respiratory disease. Eur. Respir. J. 19, 350-355.
150. Saito, H., Kato, A., Matsumoto, K., and Okayama, Y. (2006). Culture of human mast cells from peripheral blood progenitors. Nat. Protoc. 1, 2178-2183.
151. Samayawardhena, L. A., Hu, J., Stein, P. L., and Craig, A. W. (2006). Fyn kinase acts upstream of Shp2 and p38 mitogen-activated protein kinase to promote chemotaxis of mast cells towards stem cell factor. Cell. Signal. 18, 1447-1454.
152. Samayawardhena, L. A., Kapur, R., and Craig, A. W. (2007). Involvement of Fyn kinase in Kit and integrinmediated Rac activation, cytoskeletal reorganization, and chemotaxis of mast cells. Blood 109, 3679-3686.
153. Samayawardhena, L. A., and Pallen, C. J. (2008). Protein-tyrosine phosphatase α regulates stem cell factordependent c-Kit activation and migration of mast cells. J. Biol. Chem. 283, 29175-29185.
154. Sasaki, A. T., and Firtel, R. A. (2006). Regulation of chemotaxis by the orchestrated activation of Ras, PI3K, and TOR. Eur. J. Cell Biol. 85, 873-895.
155. Sawada, J., Shimizu, S., Tamatani, T., Kanegasaki, S., Saito, H., Tanaka, A., Kambe, N., Nakahata, T., and Matsuda, H. (2005). Stem cell factor has a suppressive activity to IgEmediated chemotaxis of mast cells. J. Immunol. 174, 3626-3632.
156. Schwab, S. R., Pereira, J. P., Matloubian, M., Xu, Y., Huang, Y., and Cyster, J. G. (2005). Lymphocyte sequestration through S1P lyase inhibition and disruption of S1P gradients. Science 309, 1735-1739.
157. Scott, K., and Bradding, P. (2005). Human mast cell chemokines receptors: implications for mast cell tissue localization in asthma. Clin. Exp. Allergy 35, 693-697.
158. Shiraishi, Y., Asano, K., Nakajima, T., Oguma, T., Suzuki, Y., Shiomi, T., Sayama, K., Niimi, K., Wakaki, M., Kagyo, J., Ikeda, E., Hirai, H., Yamaguchi, K., and Ishizaka, A. (2005). Prostaglandin D2-induced eosinophilic airway inflammation is mediated by CRTH2 receptor. J. Pharmacol. Exp. Ther. 312, 954-960.
159. Sieh, M., Batzer, A., Schlessinger, J., and Weiss, A. (1994). GRB2 and phospholipase C-γ1 associate with a 36to 38-kilodalton phosphotyrosine protein after T-cell receptor stimulation. Mol. Cell Biol. 14, 4435-4442.
160. Smith, J. A., Samayawardhena, L. A., and Craig,A. W. (2010). Fps/Fes proteintyrosine kinase regulates mast cell adhesion and migration downstream of Kit and β1 integrin receptors. Cell. Signal. 22, 427-436.
161. Subramanian, K. K., Jia, Y., Zhu, D., Simms, B. T., Jo, H., Hattori, H., You, J., Mizgerd, J. P., and Luo, H. R. (2007). Tumor suppressor PTEN is a physiologic suppressor of chemoattractant-mediated neutrophil functions. Blood 109, 4028-4037.
162. Sullivan, R., Price, L. S., and Koffer, A. (1999). Rho controls cortical F-actin disassembly in addition to, but independently of, secretion in mast cells. J. Biol. Chem. 274, 38140-38146.
163. Takeda, K., Sasaki, A. T., Ha, H., Seung, H. A., and Firtel, R. A. (2007). Role of phosphatidylinositol 3-kinases in chemotaxis in Dictyostelium. J. Biol. Chem. 282, 11874-11884.
164. Taub, D., Dastych, J., Inamura, N., Upton, J., Kelvin, D., Metcalfe, D., and Oppenheim, J. (1995). Bone marrow-derived murine mast cells migrate, but do not degranulate, in response to chemokines. J. Immunol. 154, 2393-2402.
165. Taylor, M. L., Dastych, J., Sehgal, D., Sundstrom, M., Nilsson, G., Akin, C., Mage, R. G., and Metcalfe, D. D. (2001). The Kit-activating mutation D816V enhances stem cell factordependent chemotaxis. Blood 98, 1195-1199.
166. Timokhina, I., Kissel, H., Stella, G., and Besmer, P. (1998). Kit signaling through PI 3-kinase and Src kinase pathways: an essential role for Rac1 and JNK activation in mast cell proliferation. EMBO J. 17, 6250-6262.
167. Toda, A., Yokomizo, T., and Shimizu, T. (2002). Leukotriene B4 receptors. Prostaglandins Other Lipid Mediat. 68-69, 575-585.
168. Toda, M., Dawson, M., Nakamura, T., Munro, P. M., Richardson, R. M., Bailly, M., and Ono, S. J. (2004). Impact of engagement of FcεRI and CC chemokine receptor 1 on mast cell activation and motility. J. Biol. Chem. 279, 48443-48448.
169. Trub, T., Frantz, J. D., Miyazaki, M., Band, H., and Shoelson, S. E. (1997). The role of a lymphoid-restricted, Grb2-like SH3-SH2-SH3 protein in T cell receptor signaling. J. Biol. Chem. 272, 894-902.
170. Tsai, M., Takeishi, T., Thompson, H., Langley, K. E., Zsebo, K. M., Metcalfe, D. D., Geissler, E. N., and Galli, S. J. (1991). Induction of mast cell proliferation, maturation, and heparin synthesis by the rat c-kit ligand, stem cell factor. Proc. Natl. Acad. Sci. U.S.A. 88, 6382-6386.
171. Tu̇ mová, M., Koffer, A., Šimíček, M., Dráberova, L., and Dráber, P. (2010). The transmembrane adaptor protein NTAL signals to mast cell cytoskeleton via the small GTPase Rho. Eur. J. Immunol. 40, 3235-3245.
172. Ueda, S., Mizuki, M., Ikeda, H., Tsujimura, T., Matsumura, I., Nakano, K., Daino, H., Honda, Z. Z., Sonoyama, J., Shibayama, H., Sugahara, H., Machii, T., and Kanakura, Y. (2002). Critical roles of c-Kit tyrosine residues 567 and 719 in stem cell factor-induced chemotaxis: contribution of src family kinase and PI3-kinase on calcium mobilization and cell migration. Blood 99, 3342-3349.
173. Urtz, N., Olivera, A., Bofill-Cardona, E., Csonga, R., Billich, A., Mechtcheriakova, D., Bornancin, F., Woisetschläger, M., Rivera, J., and Baumruker, T. (2004). Early activation of sphingosine kinase in mast cells and recruitment to FcεRI are mediated by its interaction with Lyn kinase. Mol. Cell Biol. 24, 8765-8777.
174. Volná, P., Lebduška, P., Dráberová, L., Šímová, S., Heneberg, P., Boubelík, M., Bugajev, V., Malissen, B., Wilson, B. S., Hořejší, V., Malissen, M., and Dráber, P. (2004). Negative regulation of mast cell signaling and function by the adaptor LAB/NTAL. J. Exp. Med. 200, 1001-1013.
175. Wang, D., and Dubois, R. N. (2010). Eicosanoids and cancer. Nat. Rev. Cancer 10, 181-193.
176. Wang, X. S., and Lau, H. Y. (2006). Prostaglandin E potentiates the immunologically stimulated histamine release from human peripheral blood-derived mast cells through EP1/EP3 receptors. Allergy 61, 503-506.
177. Wang, Y., Chen, C. L., and Iijima, M. (2011). Signaling mechanisms for chemotaxis. Dev. Growth Differ. 53, 495-502.
178. Weller, C. L., Collington, S. J., Brown, J. K., Miller, H. R., Al-Kashi, A., Clark, P., Jose, P. J., Hartnell, A., and Williams, T. J. (2005). Leukotriene B4, an activation product of mast cells, is a chemoattractant for their progenitors. J. Exp. Med. 201, 19611971.
179. Weller, C. L., Collington, S. J., Hartnell, A., Conroy, D. M., Kaise, T., Barker, J. E., Wilson, M. S., Taylor, G. W., Jose, P. J., and Williams, T. J. (2007). Chemotactic action of prostaglandin E2 on mouse mast cells acting via the PGE2 receptor 3. Proc. Natl. Acad. Sci. U.S.A. 104, 11712-11717.
180. Wrzesinski, S. H., Wan, Y. Y., and Flavell, R. A. (2007). Transforming growth factor-β and the immune response: implications for anticancer therapy. Clin. Cancer Res. 13, 5262-5270.
181. Yamamoto, Y., Otani, S., Hirai, H., Nagata, K., Aritake, K., Urade, Y., Narumiya, S., Yokozeki, H., Nakamura, M., and Satoh, T. (2011). Dual functions of prostaglandin D2 in murine contact hypersensitivity via DP and CRTH2. Am. J. Pathol. 179, 302-314.
182. Yamashita, T., Mao, S.-Y., and Metzger, H. (1994). Aggregation of the high-affinity IgE receptor and enhanced activity of p53/p56lyn protein-tyrosine kinase. Proc. Natl. Acad. Sci. U.S.A. 91, 1125111255.
183. Yokomizo, T. (2011). Leukotriene B4 receptors: novel roles in immunological regulations. Adv. Enzyme Regul. 51, 59-64.
184. Yokomizo, T., Izumi, T., Chang, K., Takuwa, Y., and Shimizu, T. (1997). A G-protein-coupled receptor for leukotriene B4 that mediates chemotaxis. Nature 387, 620-624.
185. Yokomizo, T., Kato, K., Terawaki, K., Izumi, T., and Shimizu, T. (2000). A second leukotriene B4 receptor, BLT2. A new therapeutic target in inflammation and immunological disorders. J. Exp. Med. 192, 421-432.
186. Zhang, W., Sloan-Lancaster, J., Kitchen, J., Trible, R. P., and Samelson, L. E. (1998). LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell 92, 83-92.
187. Zhong, H., Shlykov, S. G., Molina, J. G., Sanborn, B. M., Jacobson, M. A., Tilley, S. L., and Blackburn, M. R. (2003). Activation of murine lung mast cells by the adenosine A3 receptor. J. Immunol. 171, 338-345.
188. Zhu, M., Liu,Y., Koonpaew, S., Granillo, O., and Zhang, W. (2004). Positive and negative regulation of FcεRImediated signaling by adaptor protein LAB/NTAL. J. Exp. Med. 200, 991-1000.
189. Zlotnik, A., and Yoshie, O. (2000). Chemokines: a new classification system and their role in immunity. Immunity 12, 121-127.
190. Zudaire, E., Martínez, A., Garayoa, M., Pío, R., Kaur, G., Woolhiser, M. R., Metcalfe, D. D., Hook, W. A., Siraganian, R. P., Guise, T. A., Chirgwin, J. M., and Cuttitta, F. (2006). Adrenomedullin is a cross-talk molecule that regulates tumor and mast cell function during human carcinogenesis. Am. J. Pathol. 168, 280-291.